In recent years, machine learning approaches have been successfully applied for analysis of neuroimaging data, to help in the context of disease diagnosis. We provide, in this paper, an overview of recent support vector machine-based methods developed and applied in psychiatric neuroimaging for the investigation of schizophrenia. In particular, we focus on the algorithms implemented by our group, which have been applied to classify subjects affected by schizophrenia and healthy controls, comparing them in terms of accuracy results with other recently published studies. First we give a description of the basic terminology used in pattern recognition and machine learning. Then we separately summarize and explain each study, highlighting the main features that characterize each method. Finally, as an outcome of the comparison of the results obtained applying the described different techniques, conclusions are drawn in order to understand how much automatic classification approaches can be considered a useful tool in understanding the biological underpinnings of schizophrenia. We then conclude by discussing the main implications achievable by the application of these methods into clinical practice. 1. Introduction Investigating the neurobiological bases of psychiatric disorders requires a large sample studied in a longitudinal perspective from early stages of the diseases. In this context, magnetic resonance imaging (MRI) is the gold-standard technique to explore the anatomical and functional underpinnings of such illnesses [1–3]. In order to accurately analyze such large amount of imaging data, automated methods are becoming essential [4]. As outlined by Lao and colleagues [5], to develop an accurate detector of pathology from a set of images, two issues need to be addressed. First, an image analysis methodology is needed in order to extract the most relevant information from the images. Second, a pattern classification method has to be designed to process the extracted information, in order to determine the likelihood of the disease. Feature extraction is aimed at characterizing an object in terms of properties, or features, such as dimensions, shape, color, and texture. Chosen features are those that, when belonging to objects of the same category, or class, are very similar; on the contrary, they should be very different from objects in different categories. The set of features extracted from an object can be considered as a signature which describes the object itself. Features are usually organized in the so-called feature vector, a vector of arbitrary
References
[1]
P. R. Szeszko, K. L. Narr, O. R. Phillips et al., “Magnetic resonance imaging predictors of treatment response in first-episode schizophrenia,” Schizophrenia Bulletin, vol. 38, no. 3, pp. 569–578, 2012.
[2]
B. Olabi, I. Ellison-Wright, A. M. McIntosh, S. J. Wood, E. Bullmore, and S. M. Lawrie, “Are there progressive brain changes in schizophrenia? A meta-analysis of structural magnetic resonance imaging studies,” Biological Psychiatry, vol. 70, no. 1, pp. 88–96, 2011.
[3]
M. Bodnar, A. M. Achim, A. K. Malla, R. Joober, A. Benoit, and M. Lepage, “Functional magnetic resonance imaging correlates of memory encoding in relation to achieving remission in first-episode schizophrenia,” The British Journal of Psychiatry, vol. 200, no. 4, pp. 300–307, 2012.
[4]
S. Kl?ppel, A. Abdulkadir, C. R. Jack Jr., N. Koutsouleris, J. Mour?o-Miranda, and P. Vemuri, “Diagnostic neuroimaging across diseases,” Neuroimage, vol. 61, no. 2, pp. 457–463, 2012.
[5]
Z. Lao, D. Shen, Z. Xue, B. Karacali, S. M. Resnick, and C. Davatzikos, “Morphological classification of brains via high-dimensional shape transformations and machine learning methods,” NeuroImage, vol. 21, no. 1, pp. 46–57, 2004.
[6]
F. Pereira, T. Mitchell, and M. Botvinick, “Machine learning classifiers and fMRI: a tutorial overview,” NeuroImage, vol. 45, no. 1, pp. S199–S209, 2009.
[7]
S. Lemm, B. Blankertz, T. Dickhaus, and K.-R. Müller, “Introduction to machine learning for brain imaging,” NeuroImage, vol. 56, no. 2, pp. 387–399, 2011.
[8]
V. N. Vapnik, The Nature of Statistical Learning Theory, Springer, New York, NY, USA, 1995.
[9]
C. J. C. Burges, “A tutorial on support vector machines for pattern recognition,” Data Mining and Knowledge Discovery, vol. 2, no. 2, pp. 121–167, 1998.
[10]
M. Pontil and A. Verri, “Support vector machines for 3D object recognition,” IEEE Transactions on Pattern Analysis and Machine Intelligence, vol. 20, no. 6, pp. 637–646, 1998.
[11]
S. Modak, S. Sharma, P. Prabhakar, A. Yadav, and V. K. Jayaraman, “Application of support vector machines in fungal genome and proteome annotation,” in Laboratory Protocols in Fungal Biology, V. K. Gupta, M. G. Tuohy, M. Ayyachamy, K. M. Turner, and A. O’Donovan, Eds., Fungal Biology, pp. 565–577, Springer, New York, NY, USA, 2013.
[12]
B. Heisele, P. Ho, J. Wu, and T. Poggio, “Face recognition: component-based versus global approaches,” Computer Vision and Image Understanding, vol. 91, no. 1-2, pp. 6–21, 2003.
[13]
X.-X. Niu and C. Y. Suen, “A novel hybrid CNN-SVM classifier for recognizing handwritten digits,” Pattern Recognition, vol. 45, no. 4, pp. 1318–1325, 2012.
[14]
B. E. Boser, I. M. Guyon, and V. N. Vapnik, “Training algorithm for optimal margin classifiers,” in Proceedings of the 5th Annual ACM Workshop on Computational Learning Theory, pp. 144–152, ACM Press, July 1992.
[15]
D. D. Cox and R. L. Savoy, “Functional magnetic resonance imaging (fMRI) “brain reading”: detecting and classifying distributed patterns of fMRI activity in human visual cortex,” NeuroImage, vol. 19, no. 2, pp. 261–270, 2003.
[16]
Z. Wang, A. R. Childress, J. Wang, and J. A. Detre, “Support vector machine learning-based fMRI data group analysis,” NeuroImage, vol. 36, no. 4, pp. 1139–1151, 2007.
[17]
G. Orrù, W. Pettersson-Yeo, A. F. Marquand, G. Sartori, and A. Mechelli, “Using support vector machine to identify imaging biomarkers of neurological and psychiatric disease: a critical review,” Neuroscience and Biobehavioral Reviews, vol. 36, no. 4, pp. 1140–1152, 2012.
[18]
J. Ashburner and K. J. Friston, “Voxel-based morphometry—the methods,” NeuroImage, vol. 11, no. 6, pp. 805–821, 2000.
[19]
C. W. Nordahl, D. Dierker, I. Mostafavi et al., “Cortical folding abnormalities in autism revealed by surface-based morphometry,” Journal of Neuroscience, vol. 27, no. 43, pp. 11725–11735, 2007.
[20]
D. Pantazis, R. M. Leahy, T. E. Nichols, and M. Styne, “Statistical surface-based morphometry using a non-parametric approach,” in Proceedings of the 2nd IEEE International Symposium on Biomedical Imaging: Macro to Nano, pp. 1283–1286, April 2004.
[21]
M. E. Shenton, C. C. Dickey, M. Frumin, and R. W. McCarley, “A review of MRI findings in schizophrenia,” Schizophrenia Research, vol. 49, no. 1-2, pp. 1–52, 2001.
[22]
D. A. N. Rujescu and D. A. Collier, “Dissecting the many genetic faces of schizophrenia,” Epidemiologia e Psichiatria Sociale, vol. 18, no. 2, pp. 91–95, 2009.
[23]
Y. Fan, D. Shen, R. C. Gur, R. E. Gur, and C. Davatzikos, “COMPARE: classification of morphological patterns using adaptive regional elements,” IEEE Transactions on Medical Imaging, vol. 26, no. 1, pp. 93–105, 2007.
[24]
G. Gerig, M. Styner, M. E. Shenton, and J. A. Lieberman, “Shape versus size: improved understanding of the morphology of brain structures,” in Proceedings of the Medical Image Computing and Computer-Assisted Intervention (MICCAI '01), pp. 24–32, 2001.
[25]
N. Koutsouleris, E. M. Meisenzahl, C. Davatzikos et al., “Use of neuroanatomical pattern classification to identify subjects in at-risk mental states of psychosis and predict disease transition,” Archives of General Psychiatry, vol. 66, no. 7, pp. 700–712, 2009.
[26]
U. Yoon, J.-M. Lee, K. Im et al., “Pattern classification using principal components of cortical thickness and its discriminative pattern in schizophrenia,” NeuroImage, vol. 34, no. 4, pp. 1405–1415, 2007.
[27]
L. Palaniyappan and P. F. Liddle, “Aberrant cortical gyrification in schizophrenia: a surface-based morphometry study,” Journal of Psychiatry & Neuroscience, vol. 37, no. 6, pp. 399–406, 2012.
[28]
U. Castellani, E. Rossato, V. Murino et al., “Classification of schizophrenia using feature-based morphometry,” Journal of Neural Transmission, vol. 119, no. 3, pp. 395–404, 2012.
[29]
U. Castellani, A. Perina, V. Murino et al., “Brain morphometry by probabilistic latent semantic analysis,” in Proceedings of the 13th international conference on Medical Image Computing and Computer-Assisted Intervention: Part II (MICCAI '10), September 2010.
[30]
A. Ula?, R. P. W. Duin, U. Castellani et al., “Dissimilarity-based detection of schizophrenia,” in Proceedings of the 1st Workshop on Brain Decoding: Pattern Recognition Challenges in Neuroimaging (WBD '10), pp. 32–35, August 2010.
[31]
U. Castellani, P. Mirtuono, V. Murino et al., “A new shape diffusion descriptor for brain classification,” in Proceedings of the 14th International Conference on Medical Image Computing and Computer-Assisted Intervention: Part II (MICCAI '11), pp. 426–433, 2011.
[32]
A. Ula?, R. P. W. Duin, U. Castellani, et al., “Dissimilarity-based detection of schizophrenia,” International Journal of Imaging Systems and Technology, vol. 21, no. 2, pp. 179–192, 2011.
[33]
A. Ula?, U. Castellani, V. Murino, M. Bellani, M. Tansella, and P. Brambilla, “Biomarker evaluation by multiple Kernel learning for schizophrenia detection,” in Proceedings of the International Workshop on Pattern Recognition in NeuroImaging (PRNI '12), pp. 89–92, July 2012.
[34]
A. Ula?, M. G?nen, U. Castellani et al., “A localized MKL method for brain classification with known intra-class variability,” in Machine Learning in Medical Imaging, F. Wang, D. Shen, P. Yan, and K. Suzuki, Eds., vol. 7588 of Lecture Notes in Computer Science, pp. 152–159, 2012.
[35]
H. Yang, J. Liu, J. Sui, G. Pearlson, and V. D. Calhoun, “A hybrid machine learning method for fusing fMRI and genetic data: combining both improves classification of schizophrenia,” Frontiers in Human Neuroscience, vol. 4, article 192, 2010.
[36]
R. O. Duda, P. E. Hart, and D. G. Stork, Pattern Classification, Springer, New York, NY, USA, 2nd edition, 2001.
[37]
J. Zhang, B. Yan, X. Huang, P. Yang, and C. Huang, “The diagnosis of Alzheimer's disease based on voxel-based morphometry and support vector machine,” in Proceedings of the 4th International Conference on Natural Computation (ICNC '08), pp. 197–201, October 2008.
[38]
H. Selvaraj, S. T. Selvi, D. Selvathi, and L. Gewali, “Brain MRI slices classification using least squares support vector machine,” International Journal of Intelligent Computing in Medical Sciences and Image Processing, vol. 1, no. 1, pp. 21–33, 2007.
[39]
S. Kloppel, A. Abdulkadir, C. R. Jack Jr., N. Koutsouleris, J. Mour?o-Miranda, and P. Vemuri, “Diagnostic neuroimaging across diseases,” Neuroimage, vol. 61, no. 2, pp. 457–463, 2012.
[40]
H. Schutze, D. A. Hull, and J. O. Pedersen, “Comparison of classifiers and document representations for the routing problem,” in Proceedings of the 18th Annual International ACM SIGIR Conference on Research and Development in Information Retrieval, pp. 229–237, July 1995.
[41]
P. S. Bradley, O. L. Mangasarian, and W. N. Street, “Feature selection via mathematical programming,” INFORMS Journal on Computing, vol. 10, no. 2, pp. 209–217, 1998.
[42]
A. W. Whitney, “A direct method of nonparametric measurement selection,” IEEE Transactions on Computers, vol. 20, no. 9, pp. 1100–1103, 1971.
[43]
T. Marill and D. M. Green, “On the effectiveness of receptors in recognition systems,” IEEE Transactions on Information Theory, vol. 9, pp. 11–17, 1963.
[44]
B. Efron, “Bootstrap methods: another look at the jackknife,” The Annals of Statistics, vol. 7, no. 1, pp. 1–26, 1979.
[45]
C.-C. Chang and C.-J. Lin, “LIBSVM: a library for support vector machines,” ACM Transactions on Intelligent Systems and Technology, vol. 2, no. 3, article 27, 2011.
[46]
L. Bottou, O. Chapelle, D. DeCoste, and J. Weston, Large Scale Kernel Machines, MIT Press, Cambridge, Mass, USA, 2007.
[47]
T. Joachims, “Training linear SVMs in linear time,” in Proceedings of the 12th ACM SIGKDD International Conference on Knowledge Discovery and Data Mining (KDD '06), pp. 217–226, August 2006.
[48]
T. Hastie, R. Tibshirani, J. Friedman, and J. Franklin, “The elements of statistical learning: data mining, inference and prediction,” The Mathematical Intelligencer, vol. 27, no. 2, pp. 83–85, 2005.
[49]
C. Davatzikos, K. Ruparel, Y. Fan et al., “Classifying spatial patterns of brain activity with machine learning methods: application to lie detection,” NeuroImage, vol. 28, no. 3, pp. 663–668, 2005.
[50]
C. Ecker, V. Rocha-Rego, P. Johnston et al., “Investigating the predictive value of whole-brain structural MR scans in autism: a pattern classification approach,” NeuroImage, vol. 49, no. 1, pp. 44–56, 2010.
[51]
J. J. Koenderink and A. J. van Doorn, “Surface shape and curvature scales,” Image and Vision Computing, vol. 10, no. 8, pp. 557–564, 1992.
[52]
T. Hofmann, “Unsupervised learning by probabilistic Latent semantic analysis,” Machine Learning, vol. 42, no. 1-2, pp. 177–196, 2001.
[53]
J. Sun, M. Ovsjanikov, and L. Guibas, “A concise and provably informative multi-scale signature based on heat diffusion,” Eurographics Symposium on Geometry Processing, vol. 28, no. 5, pp. 1383–1392, 2009.
[54]
M. Reuter, F.-E. Wolter, M. Shenton, and M. Niethammer, “Laplace-Beltrami eigenvalues and topological features of eigenfunctions for statistical shape analysis,” Computer Aided Design, vol. 41, no. 10, pp. 739–755, 2009.
[55]
D. G. Lowe, “Object recognition from local scale-invariant features,” in Proceedings of the 7th IEEE International Conference on Computer Vision (ICCV '99), pp. 1150–1157, September 1999.
[56]
G. Cruska, C. R. Dance, L. Fan, J. Willamowski, and C. Bray, “Visual categorization with bags of keypoints,” in Proceedings of the Workshop on Statistical Learning in Computer Vision (ECCV '04), pp. 1–22, 2004.
[57]
K. Grauman and T. Darrell, “The pyramid match kernel: efficient learning with sets of features,” Journal of Machine Learning Research, vol. 8, pp. 725–760, 2007.
[58]
F. R. Bach, G. R. G. Lanckriet, and M. I. Jordan, “Multiple kernel learning, conic duality, and the SMO algorithm,” in Proceedings of the 21st International Conference on Machine Learning (ICML '04), pp. 41–48, July 2004.
[59]
G. R. G. Lanckriet, N. Cristianini, P. Bartlett, L. El Ghaoui, and M. I. Jordan, “Learning the kernel matrix with semidefinite programming,” Journal of Machine Learning Research, vol. 5, pp. 27–72, 2004.
[60]
M. Gonen and E. Alpayd?n, “Multiple kernel learning algorithms,” Journal of Machine Learning Research, vol. 12, pp. 2181–2238, 2011.
[61]
N. Cristianini and J. Shawe-Taylor, An Introduction to Support Vector Machines and Other Kernel-Based Learning Methods, Cambridge University Press, 2000.
[62]
M. Kloft, U. Brefeld, S. Sonnenburg, and A. Zien, “?p-norm multiple kernel learning,” Journal of Machine Learning Research, vol. 12, pp. 953–997, 2011.
[63]
A. Rakotomamonjy, F. R. Bach, S. Canu, and Y. Grandvalet, “SimpleMKL,” Journal of Machine Learning Research, vol. 9, pp. 2491–2521, 2008.
[64]
L. G. Nyul, J. K. Udupa, and X. Zhang, “New variants of a method of MRI scale standardization,” IEEE Transactions on Medical Imaging, vol. 19, no. 2, pp. 143–150, 2000.
[65]
M. G?nen and E. Alpaydin, “Localized multiple kernel learning,” in Proceedings of the 25th International Conference on Machine Learning, pp. 352–359, Helsinki, Finland, July 2008.
[66]
R. A. Jacobs, M. I. Jordan, S. J. Nowlan, and G. E. Hinton, “Adaptive mixtures of local experts,” Neural Computation, vol. 3, no. 1, pp. 79–87, 1991.
[67]
E. Pekalska and R. P. W. Duin, The Dissimilarity Representation for Pattern Recognition. Foundations and Applications, World Scientific Publishing, 2005.
[68]
B. Scholkopf and A. J. Smola, Learning with Kernels, The MIT Press, 2002.
[69]
R. W. Freudenmann, M. K?lle, A. Huwe et al., “Delusional infestation: neural correlates and antipsychotic therapy investigated by multimodal,” Progress in Neuro-Psychopharmacology and Biological Psychiatry, vol. 34, no. 7, pp. 1215–1222, 2010.
[70]
K. J. Friston and R. J. Dolan, “Computational and dynamic models in neuroimaging,” NeuroImage, vol. 52, no. 3, pp. 752–765, 2010.